Glutamate receptors at atomic resolution

Nature

Volumn 440, Issue 7083, 2006, Pages 456-462

  Mayer, Mark L ^a  

^a Porter Neuroscience Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CRYSTALLOGRAPHY; IONS; NEUROLOGY; STRUCTURAL ANALYSIS;

AMINO-ACID GLUTAMATE; DISCRETE LIGAND-BINDING; GLUTAMATE RECEPTORS;

AMINO ACIDS;

GLUTAMATE RECEPTOR; GLUTAMIC ACID; ION CHANNEL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER;

NERVOUS SYSTEM;

ALLOSTERISM; BRAIN; CHANNEL GATING; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; CYTOPLASM; DEGENERATIVE DISEASE; DESENSITIZATION; EVOLUTION; LIGAND BINDING; MENTAL DISEASE; MOLECULAR BIOLOGY; NEUROTRANSMISSION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SPINAL CORD; STRUCTURE ANALYSIS; SYNAPSE;

EID: 33645321641     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04709     Document Type: Review

References (75)

1. Watkins, J. C. & Evans, R. H. Excitatory amino acid transmitters. Annu. Rev. Pharmacol. Toxicol. 21, 165-204 (1981).
2. Mayer, M. L. & Westbrook, G. L. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28, 197-276 (1987).
3. Collingridge, G. L. & Lester, R. A. J. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 41, 143-210 (1989).
4. Collingridge, G. L. & Bliss, T. V. Memories of NMDA receptors and LTP. Trends Neurosci. 18, 54-56 (1995).
5. 2+ permeability of AMPA receptors in principle neurons and interneurons in rat CNS. Neuron 15, 193-204 (1995).
6. Lerma, J. Roles and rules of kainate receptors in synaptic transmission. Nature Rev. Neurosci. 4, 481-495 (2003).
7. Perl, T. M. et al. An outbreak of toxic encephalopathy caused by eating mussels contaminated with domoic acid. N. Engl. J. Med. 322, 1775-1780 (1990).
8. Watkins, J. C. & Jane, D. E. The glutamate story. Br. J. Pharmacol. 147 Suppl 1, S100-S108 (2006).
9. Hollmann, M. in Ionotropic Glutamate Receptors in the CNS (eds Jonas, P. & Monyer, H.) 3-98 (Springer, Berlin, 1999).
10. Sommer, B. et al. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249, 1580-1585 (1990).
11. Sommer, B., Köhler, M., Sprengel, R. & Seeburg, P. H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19 (1991).
12. Puchalski, R. B. et al. Selective RNA editing and subunit assembly of native glutamate receptors. Neuron 13, 131-147 (1994).
13. Ayalon, G. & Stern-Bach, Y. Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 31, 103-113 (2001).
14. Ayalon, G., Segev, E., Elgavish, S. & Stern-Bach, Y. Two regions in the N-terminal domain of ionotropic glutamate receptor 3 form the subunit oligomerization interfaces that control subtype-specific receptor assembly. J. Biol. Chem. 280, 15053-15060 (2005).
15. Paoletti, P., Ascher, P. & Neyton, J. High-affinity zinc inhibition of NMDA NR1-NR2A receptors. J. Neurosci. 17, 5711-5725 (1997).
16. Perin-Dureau, F., Rachline, J., Neyton, J. & Paoletti, P. Mapping the binding site of the neuroprotectant ifenprodil on NMDA receptors. J. Neurosci. 22, 5955-5965 (2002).
17. Masuko, T. et al. A regulatory domain (R1-R2) in the amino terminus of the N-methyl-D-aspartate receptor: effects of spermine, protons, and ifenprodil, and structural similarity to bacterial leucine/isoleucine/valine binding protein. Mol. Pharmacol. 55, 957-969 (1999).
18. Paoletti, P. et al. Molecular organization of a zinc binding N-terminal modulatory domain in a NMDA receptor subunit. Neuron 28, 911-925 (2000).
19. Pasternack, A. et al. Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain. J. Biol. Chem. 277, 49662-49667 (2002).
20. Stern-Bach, Y. et al. Agonist-selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid binding proteins. Neuron 13, 1345-1357 (1994).
21. Kuusinen, A., Arvola, M. & Keinanen, K. Molecular dissection of the agonist binding site of an AMPA receptor. EMBO J. 14, 6327-6332 (1995).
22. Chen, G. Q., Sun, Y., Jin, R. & Gouaux, E. Probing the ligand binding domain of the GluR2 receptor by proteolysis and deletion mutagenesis defines domain boundaries and yields a crystallizable construct. Protein Sci. 7, 2623-2630 (1998).
23. + channels examined by scanning mutagenesis. J. Gen. Physiol. 117, 345-360 (2001).
24. + channels and ionotropic glutamate receptors? Trends Neurosci. 26, 27-32 (2003).
25. Chen, G. Q., Cui, C., Mayer, M. L. & Gouaux, E. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402, 817-821 (1999).
26. Sobolevsky, A. I., Yelshansky, M. V. & Wollmuth, L. P. The outer pore of the glutamate receptor channel has 2-fold rotational symmetry. Neuron 41, 367-378 (2004).
27. Soderling, T. R. & Derkach, V. A. Postsynaptic protein phosphorylation and LTP. Trends Neurosci. 23, 75-80 (2000).
28. Tavalin, S. J. et al. Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J. Neurosci. 22, 3044-3051 (2002).
29. Vissel, B., Krupp, J. J., Heinemann, S. F. & Westbrook, G. L. Intracellular domains of NR2 alter calcium-dependent inactivation of N-methyl-D-aspartate receptors. Mol. Pharmacol. 61, 595-605 (2002).
30. Peng, J. et al. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 279, 21003-21011 (2004).
31. Mano, I., Lamed, Y. & Teichberg, V. I. A venus flytrap mechanism for activation and desensitization of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors. J. Biol. Chem. 271, 15299-15302 (1996).
32. Quiocho, F. A. & Ledvina, P. S. Atomic structure and specificity of bacterial periplasmic receptors for active transport and chemotaxis: variation of common themes. Mol. Microbiol. 20, 17-25 (1996).
33. Mayer, M. L., Olson, R. & Gouaux, E. Mechanisms for ligand binding to GluR0 ion channels: crystal structures of the glutamate and serine complexes and a closed apo state. J. Mol. Biol. 311, 815-836 (2001).
34. Watkins, J. C., Krogsgaard-Larsen, P. & Honoré, T. Structure-activity relationships in the development of excitatory amino acid receptor agonists and competitive antagonists. Trends Pharmacol. Sci. 11, 25-33 (1990).
35. Furukawa, H. & Gouaux, E. Mechanisms of activation, inhibition and specificity: crystal structures of NR1 ligand-binding core. EMBO J. 22, 1-13 (2003).
36. Mayer, M. L. Crystal structures of the GluR5 and GluR6 ligand binding cores: molecular mechanisms underlying kainate receptor selectivity. Neuron 45, 539-552 (2005).
37. Armstrong, N. & Gouaux, E. Mechanisms for activation and antagonism of an AMPA-sensitive glutamate receptor: Crystal structures of the GluR2 ligand binding core. Neuron 28, 165-181 (2000).
38. Jin, R., Banke, T. G., Mayer, M. L., Traynelis, S. F. & Gouaux, E. Structural basis for partial agonist action at ionotropic glutamate receptors. Nature Neurosci. 6, 803-810 (2003).
39. Hogner, A. et al. Structural basis for AMPA receptor activation and ligand selectivity: Crystal structures of five agonist complexes with the GluR2 ligand-binding core. J. Mol. Biol. 322, 93-109 (2002).
40. Mayer, M. L., Ghosal, A. K., Dolman, N. P. & Jane, D. E. Crystal structures of the kainate receptor GluR5 ligand binding core dimer with novel GluR5 selective antagonists. J. Neurosci. 26, 2850-2859 (2006).
41. Colquhoun, D. & Ogden, D. C. Activation of ion channels in the frog end-plate by high concentrations of acetylcholine. J. Physiol. (Lond.) 395, 31-159 (1988).
42. Rosenmund, C., Stern-Bach, Y. & Stevens, C. F. The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599 (1998).
43. Armstrong, N., Mayer, M. & Gouaux, E. Tuning activation of the AMPA-sensitive GluR2 ion channel by genetic adjustment of agonist-induced conformational changes. Proc. Natl Acad. Sci. USA 100, 5736-5741 (2003).
44. Inanobe, A., Furukawa, H. & Gouaux, E. Mechanism of partial agonist action at the NR1 subunit of NMDA receptors. Neuron 47, 71-84 (2005).
45. Erreger, K. et al. Mechanism of partial agonism at NMDA receptors for a conformationally restricted glutamate analog. J. Neurosci. 25, 7858-7866 (2005).
46. Chen, P. E. et al. Structural features of the glutamate binding site in recombinant NR1/NR2A N-methyl-D-aspartate receptors determined by site-directed mutagenesis and molecular modeling. Mol. Pharmacol. 67, 1470-1484 (2005).
47. Furukawa, H., Singh, S. K., Mancusso, R. & Gouaux, E. Subunit arrangement and function in NMDA receptors. Nature 438, 185-192 (2005).
48. Mamonova, T., Hespenheide, B., Straub, R., Thorpe, M. F. & Kurnikova, M. Protein flexibility using constraints from molecular dynamics simulations. Phys. Biol. 2, S137-S147 (2005).
49. Arinaminpathy, Y., Sansom, M. S. & Biggin, P. C. Binding site flexibility: Molecular simulation of partial and full agonists with a glutamate receptor. Mol. Pharmacol. 69, 5-12 (2006).
50. Jiang, Y. et al. The open pore conformation of potassium channels. Nature 417, 523-526 (2002).
51. Banke, T. G. & Traynelis, S. F. Activation of NR1/NR2B NMDA receptors. Nature Neurosci. 6, 144-152 (2003).
52. Schorge, S., Elenes, S. & Colquhoun, D. Maximum likelihood fitting of single channel NMDA activity with a mechanism composed of independent dimers of subunits. J. Physiol. 569, 395-418 (2005).
53. Sun, Y. et al. Mechanism of glutamate receptor desensitization. Nature 417, 245-253 (2002).
54. Horning, M. S. & Mayer, M. L. Regulation of AMPA receptor gating by ligand binding core dimers. Neuron 41, 379-388 (2004).
55. Partin, K. M., Fleck, M. W. & Mayer, M. L. AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, aniracetam, and thiocyanate. J. Neurosci. 16, 6634-6647 (1996).
56. Jin, R. et al. Mechanism of positive allosteric modulators acting on AMPA receptors. J. Neurosci. 25, 9027-9036 (2005).
57. Yelshansky, M. V., Sobolevsky, A. I., Jatzke, C. & Wollmuth, L. P. Block of AMPA receptor desensitization by a point mutation outside the ligand-binding domain. J. Neurosci. 24, 4728-4736 (2004).
58. Holm, M. M. et al. A binding site tyrosine shapes desensitization kinetics and agonist potency at GluR2. A mutagenic, kinetic, and crystallographic study. J. Biol. Chem. 280, 35469-35476 (2005).
59. Lester, R. A. J., Clements, J. D., Westbrook, G. L. & Jahr, C. E. Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346, 565-567 (1990).
60. Monyer, H. et al. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221 (1992).
61. Laurie, D. J. & Seeburg, P. H. Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur. J. Pharmacol. 268, 335-345 (1994).
62. Kuner, T., Wollmuth, L. P., Karlin, A., Seeburg, P. H. & Sakmann, B. Structure of the NMDA receptor channel M2 segment inferred from the accessibility of substituted cysteines. Neuron 17, 343-352 (1996).
63. Beck, C., Wollmuth, L. P., Seeburg, P. H., Sakmann, B. & Kuner, T. NMDAR channel segments forming the extracellular vestibule inferred from the accessibility of substituted cysteines. Neuron 22, 559-570 (1999).
64. Sobolevsky, A. I., Yelshansky, M. V. & Wollmuth, L. P. State-dependent changes in the electrostatic potential in the pore of a GluR channel. Biophys. J. 88, 235-242 (2005).
65. Wollmuth, L. P. & Sobolevsky, A. I. Structure and gating of the glutamate receptor ion channel. Trends Neurosci. 27, 321-328 (2004).
66. 2+ flux rates in NMDA receptor channels. J. Neurosci. 22, 10209-10216 (2002).
67. Schorge, S. & Colquhoun, D. Studies of NMDA receptor function and stoichiometry with truncated and tandem subunits. J. Neurosci. 23, 1151-1158 (2003).
68. Balannik, V., Menniti, F. S., Paternain, A. V., Lerma, J. & Stern-Bach, Y. Molecular mechanism of AMPA receptor noncompetitive antagonism. Neuron 48, 279-288 (2005).
69. Lipton, S. A. Paradigm shift in neuroprotection by NMDA receptor blockade: Memantine and beyond. Nature Rev. Drug Discov. 5, 160-170 (2006).
70. Zuo, J. et al. Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature 388, 769-773 (1997).
71. Kohda, K., Wang, Y. & Yuzaki, M. Mutation of a glutamate receptor motif reveals its role in gating and delta2 receptor channel properties. Nature Neurosci. 3, 315-322 (2000).
72. Klein, R. M. & Howe, J. R. Effects of the lurcher mutation on GluR1 desensitization and activation kinetics. J. Neurosci. 24, 4941-4951 (2004).
73. Tomita, S. et al. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058 (2005).
74. Turetsky, D., Garringer, E. & Patneau, D. K. Stargazin modulates native AMPA receptor functional properties by two distinct mechanisms. J. Neurosci. 25, 7438-7448 (2005).
75. Priel, A. et al. Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. J. Neurosci. 25, 2682-2686 (2005).